Abstract

In eukaryotic algae, respiratory O2 uptake is enhanced after illumination, which is called light-enhanced respiration (LER). It is likely stimulated by an increase in respiratory substrates produced during photosynthetic CO2 assimilation and function in keeping the metabolic and redox homeostasis in the light in eukaryotic cells, based on the interactions among the cytosol, chloroplasts, and mitochondria. Here, we first characterize LER in photosynthetic prokaryote cyanobacteria, in which respiration and photosynthesis share their metabolisms and electron transport chains in one cell. From the physiological analysis, the cyanobacterium Synechocystis sp. PCC 6803 performs LER, similar to eukaryotic algae, which shows a capacity comparable to the net photosynthetic O2 evolution rate. Although the respiratory and photosynthetic electron transports share the interchain, LER was uncoupled from photosynthetic electron transport. Mutant analyses demonstrated that LER is motivated by the substrates directly provided by photosynthetic CO2 assimilation, but not by glycogen. Further, the light-dependent activation of LER was observed even with exogenously added glucose, implying a regulatory mechanism for LER in addition to the substrate amounts. Finally, we discuss the physiological significance of the large capacity of LER in cyanobacteria and eukaryotic algae compared to those in plants that normally show less LER.

Highlights

  • Respiration is one of the most important biological activities, even in oxygenic phototrophs that produce NAD(P)H and ATP by photosynthetic metabolism

  • The light-enhanced dark respiration, one of the most indisputable phenomena that shows respiration is linked to photosynthesis under light conditions, is associated with the amounts of respiratory substrates generated during photosynthesis in eukaryotic algae [4,13,14,15,16]

  • Since light-enhanced respiration (LER) is activated by illumination, it is difficult to analyze the capacity of LER in photosynthetic organisms that are already adapted to light

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Summary

Introduction

Respiration is one of the most important biological activities, even in oxygenic phototrophs that produce NAD(P)H and ATP by photosynthetic metabolism. The redox states of the photosynthetic electron transport components and the amounts of photosynthetic metabolites are affected in respiratory mutants [20,21,22,23,24,25,26], the interplay between respiration and photosynthesis in cyanobacterial cells. 6803), dark respiration starts from the degradation of glycogen catalyzed by debranching enzymeor phosphorylase-dependent pathways [27,28] Hexoses such as glucose are metabolized to pyruvate in the cytosol via glycolysis, similar to photosynthetic eukaryotes, and drive the cyanobacterial tricarboxylic acid (TCA) cycle in the cytosol. In the respiratory electron transport, the electrons are transported from NAD(P)H dehydrogenase (NDH)-1, NDH-2, and succinate dehydrogenase (SDH) to cytochrome c oxidase (COX), reducing O2 to H2O These two electron transport chains share the interchain components plastoquinone (PQ), the cytochrome b6/f complex, plastocyanin, and cytochrome c [18,22]. We first characterize LER in S. 6803 to deepen the understanding on the molecular mechanism of the interactions between respiration and photosynthesis in photosynthetic organisms

Results
Growth Conditions and Chl a Determination
Generation of Mutants
Measurement of O2 and Chl Fluorescence
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